Cell type specific interleukin-6 induced responses in tumor keratinocytes and stromal fibroblasts are essential for invasive growth

Int J Cancer. 2014 Aug 1;135(3):551-62. doi: 10.1002/ijc.27951. Epub 2014 Mar 14.

Abstract

Interleukin-6 (IL-6) is one of the major inflammatory interleukins that has been linked to cancer progression. In our model for human skin squamous cell carcinoma (SCC), IL-6 expression is strongly upregulated upon progression from benign tumors to highly malignant, metastasizing SCCs. We now demonstrate that IL-6 promotes malignant and invasive tumor growth in human skin SCCs by inducing cell type specific cytokine profiles in tumor keratinocytes and stromal fibroblasts, activating the latter towards a tumor associated fibroblast (TAF) phenotype. In three-dimensional organotypic cocultures in vitro invasive growth of IL-6 overexpressing tumor keratinocytes, is associated with increased expression of matrix metalloproteinase-2 (MMP-2), MMP-14 and tissue inhibitor of metalloproteinases-2, and clearly depends on IL-6 activated fibroblasts. IL-6-induced secretion of monocyte chemotactic protein-1 (MCP-1) in tumor keratinocytes and of hepatocyte growth factor in fibroblasts is crucial for regulating expression and activation of MMP-2. This functional role of IL-6 is confirmed in vivo. Here MMP-14 and MMP-2 expression occur exclusively in surface transplants of IL-6 overexpressing keratinocytes and fibroblasts are identified as important source of MMP-2. Our data indicate that tumor keratinocytes derived IL-6 activates stromal fibroblasts towards a TAF phenotype, promoting tumor invasion via enhanced expression and activation of MMP-2.

Keywords: MMP; SCC; fibroblasts; growth factor network; interleukin-6; tumor progression.

MeSH terms

  • Animals
  • Carcinoma, Squamous Cell / metabolism
  • Carcinoma, Squamous Cell / pathology*
  • Cell Adhesion
  • Cell Communication
  • Cell Movement
  • Cells, Cultured
  • Coculture Techniques
  • Culture Media, Conditioned / pharmacology
  • Fibroblasts / metabolism
  • Fibroblasts / pathology*
  • Flow Cytometry
  • Fluorescent Antibody Technique, Indirect
  • Humans
  • In Situ Hybridization
  • Interleukin-6 / metabolism*
  • Keratinocytes / metabolism
  • Keratinocytes / pathology*
  • Matrix Metalloproteinase 2 / metabolism
  • Mice
  • Mice, Nude
  • Neoplasm Invasiveness
  • Skin Neoplasms / metabolism
  • Skin Neoplasms / pathology*
  • Stromal Cells / metabolism
  • Stromal Cells / pathology*

Substances

  • Culture Media, Conditioned
  • Interleukin-6
  • MMP2 protein, human
  • Matrix Metalloproteinase 2